The case of the missing genitalia: copulation costs for male spiders

This post is written by Chris Buddle (Associate Professor, McGill University). This article was originally published in “The Canadian Arachnologist” – a newsletter about Arachnology in Canada (this newsletter is no longer being published).

Spider sex can be a dangerous and costly venture, the classic example being the (often) misunderstood act of sexual cannibalism (e.g., the black widow spider). However, many of the costs for males are not always so obvious: during copulation, the emboli of some male spiders may break off, which results in the male being unable to properly re-fill his palpal organ and mate again (Foelix 1996). Without this ability, the male’s future is essentially an early retirement. While sorting and identifying spiders for my dissertation research, I noticed that male Cybaeopsis euopla(a ‘hackledmesh’ weaver spider) seemed to frequently be missing one or both of their pedipalps. Could this be another example of a copulation cost?

Looking to the literature, missing pedipalps are documented with some species – tiny males from the sexually dimorphic genus Tidarren (Theridiidae) will remove their own palps and this increases their running speed considerably (Ramos et al. 2004). Working with the same genus, Knofach and van Harten (2001) observed that females remove one of the male’s palps ‘after achieving genitalia coupling’. The female then proceeds to eat the male, while the detached palp acts as both a mating plug and continues to inseminate the female! Something similar happens with the species Nephilengys malabarensis and this fascinating biology was reported by science bloggers such as Ed Yong. In the wolf spider (Lycosidae) Pardosa milvina, frequent palpal losses were observed and effects on courtship and mating were studied by Lynam et al. (2006). Perhaps not surprisingly, these authors report that ‘intact males were less likely to be cannibalized and suffered fewer predatory attacks by females than autotomized males’.

With that background, I began counting the frequency of missing pedipalps for a sub-sample of the specimens of C. euopla. The objective was to assess the percentage of males were missing right, left, or both pedipalps and see if this related to phenology or other life-history events.

The samples came from a mixed-wood forest at the George Lake Field Station, located about 75 km NW of Edmonton, Alberta. This mature mixed-wood forest is dominated by trembling aspen and balsam poplar. Samples were collected using standard pitfall traps, and were part of several other projects on spider assemblages in mixed-wood boreal forests (e.g., see Buddle 2001).

Cybaeopsis euopla – lovely little spiders! (Photo by C. Buddle)

Cybaeopis euopla (Amaurobiidae) (formerly Callioplus euoplus) is widespread in Canada, ranging from the Maritimes to the far north-west (Leech 1972). Males are about 3.5 to 5 mm in length, and are pale orange to light brown in colour. Specimens are typically collected from the leaf-litter of closed-canopy deciduous forests (Leech 1972; Buddle et al. 2000). From a sample of 653 male C. euopla, I found a total of 309 (or 47%) to be missing either one or both pedipalps. This is an impressive number, and essentially means that about half the males in the population are missing the very parts of their bodies that are required for reproduction. Of the 309 that were missing pedipalps, 124 were missing the left pedipalp, 97 were missing the right pedipalp, and 88 were missing both. In virtually all cases, the pedipalp was severed at the trochanter-femur joint. So the most plausible explanations for missing pedipalps are:

Pedipalp autotomy occurs during the act of copulation

The female may remove the pedipalps before, during or after copulation

C. euopla males may use their pedipalps in antagonistic courtship behaviours

Perhaps pedipalps are frequently used to grapple with aggressive prey, and are thus damaged.

It would be difficult to relate missing pedipalps to the act of copulation without detailed studies of courtship and copulation in C. euopla. However, the fate of pedipalps could be determined indirectly if the frequency of missing pedipalps increased during the reproductive period. The period of reproduction for ground-dwelling spiders, such as C. euopla, can be assessed from the peak activity period for male and female spiders, inferred from a passive sampling technique such as pitfall trapping. Using a larger data-set for male and female C. euopla collected by pitfall traps set at the George Lake Field Station, it is evident that males are most active early in the season (early May through the end of June) (Figure 1). Females were found throughout the spring and summer months over two years, with a slight increase in late June (Figure 1). These results generally agree with Leech (1972), who suggests May and June are the main periods of activity for C. euopla. Thus, it is inferred that this species will mate primarily in the spring in central Alberta.

The next step is to ask whether the frequency of missing pedipalps is related to the hypothesized mating period. This was done by calculating the average percentage of males with missing pedipalps as a function of sampling date (Figure 2). In both sampling years, the percentage of males with missing pedipalps increased as the season progressed (Figure 2). Although the sample size for July samples was low (12 individuals), the average number missing pedipalps was over 80%. Furthermore, the earliest sampling date in 1999 (6 May), which collected over 200 individuals, had the lowest average percentage of males with missing pedipalps (< 20%). These results indirectly suggest that as the season progresses, and the spiders mate, males begin to lose their pedipalps. I can therefore likely exclude the possibility that palpal loss is related to aggressive prey, and the explanation is likely related to courtship or copulation.

This small study has raised as many questions as it has answered, and there are certainly other explanations that I have failed to mention. I invite fellow Arachnologists to comment on the phenomenon of missing pedipalps in C. euopla, and in other species. I suspect pedipalp loss is widespread, but seriously understudied. Given this importance of palps to the fitness of spiders, future research is certainly warranted.

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Fascinating, Chris. At a deeper level, does anyone have hypotheses for how, why, and when palpal organs and this method of copulation evolved in the first place? I haven’t seen any, but I should look more thoroughly. Any thoughts?